Phylogeography of the Sand Dune Ant Mycetophylax
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Cardoso et al. BMC Evolutionary Biology (2015) 15:106 DOI 10.1186/s12862-015-0383-4 RESEARCH ARTICLE Open Access Phylogeography of the sand dune ant Mycetophylax simplex along the Brazilian Atlantic Forest coast: remarkably low mtDNA diversity and shallow population structure Danon Clemes Cardoso1,2,3*, Maykon Passos Cristiano3,4, Mara Garcia Tavares1, Christoph D. Schubart3 and Jürgen Heinze3* Abstract Background: During past glacial periods, many species of forest-dwelling animals experienced range contractions. In contrast, species living outside such moist habitats appear to have reacted to Quaternary changes in different ways. The Atlantic Forest represents an excellent opportunity to test phylogeographic hypotheses, because it has a wide range of vegetation types, including unforested habitats covered predominantly by herbaceous and shrubby plants, which are strongly influenced by the harsh environment with strong wind and high insolation. Here, we investigated the distribution of genetic diversity in the endemic sand dune ant Mycetophylax simplex across its known range along the Brazilian coast, with the aim of contributing to the understanding of alternative phylogeographic patterns. We used partial sequences of the mitochondrial gene cytochrome oxidase I and nuclear gene wingless from 108 specimens and 51 specimens, respectively, to assess the phylogeography and demographic history of this species. To achieve this we performed different methods of phylogenetic and standard population genetic analyses. Results: The observed genetic diversity distribution and historical demographic profile suggests that the history of M. simplex does not match the scenario suggested for other Atlantic Forest species. Instead, it underwent demographic changes and range expansions during glacial periods. Our results show that M. simplex presents a shallow phylogeographic structure with isolation by distance among the studied populations, living in an almost panmictic population. Our coalescence approach indicates that the species maintained a stable population size until roughly 75,000 years ago, when it underwent a gradual demographic expansion that were coincident with the low sea-level during the Quaternary. Such demographic events were likely triggered by the expansion of the shorelines during the lowering of the sea level. Conclusions: Our data suggest that over evolutionary time M. simplex did not undergo dramatic range fragmentation, but rather it likely persisted in largely interconnected populations. Furthermore, we add an important framework about how both glacial and interglacial events could positively affect the distribution and diversification of species. The growing number of contrasting phylogeographic patterns within and among species and regions have shown that Quaternary events influenced the distribution of species in more ways than first supposed. Keywords: Brazilian Atlantic Forest, Mycetophylax simplex, Formicidae, Neotropical region, Gene flow, Genetic structure, Sand dunes, Restinga, Sea-level changes * Correspondence: [email protected]; Juergen. [email protected] 1Present address: Departamento de Genética, Universidade Federal do Paraná, Setor de Ciências Biológicas, Rua Francisco H. dos Santos, s/n°, Jardim das Américas, Curitiba, Paraná 81530-000, Brazil 3Zoology/Evolutionary Biology, Universität Regensburg, Universitätstrasse 31, D-93040 Regensburg, Germany Full list of author information is available at the end of the article © 2015 Cardoso et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cardoso et al. BMC Evolutionary Biology (2015) 15:106 Page 2 of 13 Background with the cyclical shrinking or expanding of forests. Alter- Climatic fluctuations during the late Quaternary associ- natively, their distribution may have remained largely ated with the Last Glacial Maximum have had a strong unchanged during these historical events. While several impact on the current distribution of many animal and species associated with humid forest environments have plant species worldwide. Climate change not only af- been used to infer the evolutionary processes that oc- fected the landscape of continental areas but also the sea curred during the Quaternary in the Atlantic Forest, only level, which in turn shaped coastal landscapes by form- a few studies have addressed organisms – exclusively ing land bridges, islands, sand coastal plains, as well as plants – associated with dry environments (see [17]). connecting and separating areas [1, 2]. All these climate- Mycetophylax simplex is a small fungus-growing ant linked processes may have influenced the evolutionary (Formicidae: Myrmicinae) endemic to sand dune envi- history of the species, especially those inhabiting coastal ronments along the Brazilian coast, occurring from the areas [3, 4]. southern São Paulo State to Rio Grande do Sul [22, 23]. Pollen data, fossil records, and paleoclimatic data indi- Although this ant exhibits a wide distribution, it is re- cate that numerous taxa in the Northern hemisphere stricted to specialized habitats (sand dunes), making it a were restricted during the period of glaciation to south- good model organism to test phylogeographic scenarios ern or eastern refugia [5], and phylogeographic studies for open and dry coastal environments. Thus, the aim of show how expansion from these sites has molded their this study is to evaluate the genetic relationship among distribution today [6–9]. In contrast, less is known about populations of M. simplex across its whole distribution these phenomena in the Southern hemisphere, where and to infer how the Quaternary oscillations affected the glacial refugia hypothesis only recently has been for- genetic diversity and structure of its populations. Based mally evaluated [10, 11]. It is presently the most frequently on DNA sequences of the mitochondrial gene cyto- suggested mechanism for the current distribution of spe- chrome oxidase subunit I (COI) and the nuclear gene cies diversity in the Brazilian Atlantic Forest (AF), the sec- wingless, we aimed to test if (i) M. simplex underwent a ond largest Neotropical forest after the Amazon rainforest. persistent range and population size during the climatic The AF extends more than 3300 km along the eastern oscillations of the Quaternary and if and how (ii) its coast of Brazil. It has received worldwide attention be- demographic history was affected by the cyclic changes cause of its high biodiversity and high level of endemism in the sea level. and was determined as one of the 25 world biodiversity hotspots for conservation priorities [10, 12]. The AF pre- Methods sents a wide range of vegetation types with conspicuous Sampling and laboratory procedures changes across landscapes, which include open habitats A total of 108 colonies of M. simplex, spanning its whole covered predominantly by herbaceous and shrubby plants, distribution area, were collected from January to September which develop on marine deposits. Despite an increasing 2011 (Fig. 1). The geographical references and sample size number of phylogeographic studies, the knowledge about of all samples are given in Table 1. The specimens were the evolutionary history of the AF is still limited and con- preserved in 100 % ethanol until DNA extraction. Whole troversial [10, 13–19]. The refugia hypothesis has gained genomic DNA was extracted from one individual per support by a growing number of phylogeographic studies colony. Genomic DNA was isolated using proteinase K di- that attempt to explain the high diversity in the AF [13, gestion followed by a standard CTAB protocol [24]. Frag- 15, 16]. Basically, it states that during glaciation, when the ments of the mitochondrial gene cytochrome oxidase climate was drier in the Southern hemisphere, forests subunit I (COI) and the nuclear gene wingless, both contracted and persisted only in moister areas, which be- known to be useful in intra-specific studies in ants (e.g. came refugia for humidity-dependent species. By vicariant [25]), were amplified by PCR using the previously pub- processes, these refugia promoted speciation and therefore lished primers LCO1490 [26] and Ben [27] for COI and today harbor a higher genetic diversity and endemism Wg578F [28] and Wg1032R [29] for wingless.DNA- than areas that did not serve as refugia [1]. amplification was conducted in reactions with 25 μLfinal The retreat of forests and the changed global climate volume containing: MgCl2 (2.5 mM), buffer (10x; Pro- conditions may have allowed the expansion of drought- mega), dNTPs (1 mM each), two primers (0.48 μMeach), tolerant biomes [20, 21]. Species adapted to dry and Taq polymerase (2 U of GoTaq® Flexi DNA Polymerase) open habitats in southern and eastern South America, and 1 μL of template DNA. PCR cycling conditions were including the Atlantic coast, may have expanded during as follows: initial denaturation for 2 min at 94 °C, then the drier periods throughout climatic oscillations. Com- 35 cycles with 94 °C for 1 min denaturation, 50 °C (COI) pared to species restricted to refugia, such species may or 55 °C (wingless)